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1 BOL MUS BIOL MELLO LEITÃO (N SÉR ) 11/12: JUNHO DE Non-volant mammals of the Estação Biológica de Santa Lúcia and adjacent areas of Santa Teresa, Espírito Santo, Brazil Marcelo Passamani 1, 2 ; Sérgio L Mendes 1,3 & Adriano G Chiarello 1 ABSTRACT: This paper presents a preliminary inventory of non-volant mammals of Estação Biológica de Santa Lúcia (EBSL) and other remnants of Atlantic forest located in Santa Teresa municipality, southeastern Brazil In EBSL, 21 species of small mammals were captured in different areas, from March 1989 to February 1990, at irregular intervals, using traps placed on the ground and fixed on branches and tree platforms The occurrence of the remaining species were confirmed through direct and indirect evidences recorded during diurnal and nocturnal censuses, as well as through a review of the museum specimens collected in Santa Teresa municipality that are deposited in the Museu de Biologia Prof Mello Leitão In total, 62 mammal species, excluding bats, were recorded for the study region This figure equals or exceeds that of most Neotropical sites, and is lower only when compared to the extremely rich mammal fauna of Manu Biosphere Reserve, Peru Considering only the Atlantic forest, the mammal richness found for Santa Teresa is also higher than all other sites already inventoried, in agreement with previous information on high tree and bird diversity recorded for the study site Key-words: Atlantic forest, Espírito Santo, mammals, survey RESUMO: Mamíferos não voadores da Estação Biológica de Santa Lúcia e arredores, Santa Teresa, Espírito Santo, Brasil Este trabalho apresenta um inventário preliminar de mamíferos não voadores da Estação Biológica de Santa Lúcia (EBSL) e outros remanescentes de Mata Atlântica do município de Santa Teresa, ES Na EBSL, os pequenos mamíferos foram inventariados em três áreas, no período de março de 1989 a fevereiro de 1990, com auxílio de armadilhas colocadas no solo e fixadas em troncos de árvores entre um e dois metros acima do solo, tendo sido capturados 1 - Museu de Biologia Prof Mello Leitão, Av José Ruschi 04, Santa Teresa, Espírito Santo, Brasil <ruschi@terra com br> 2 - Departamento de Ecologia, CCS, Universidade Federal do Rio de Janeiro, Brasil CP 68020, Ilha do Fundão, Rio de Janeiro, RJ Departamento de Biologia, UFES, Av Mal Campos, 1468, Maruípe, Vitória, Espírito Santo, <slmendes@npd ufes br>

2 202 PASSAMANI ET AL : MAMMALS OF SANTA TERESA - ES exemplares de 21 espécies As demais espécies foram assinaladas com base em contatos visuais e evidências indiretas, bem como a partir do material existente na coleção do Museu de Biologia Prof Mello Leitão (Santa Teresa - ES) Ao todo, foram encontradas 62 espécies de mamíferos para a região de estudo Este número se iguala ou excede ao da maioria das localidades neotropicais e é menor apenas que a fauna de mamíferos extremamente rica encontrada em "Manu Biosphere Reserve", Peru Considerando apenas a Mata Atlântica, a riqueza de mamíferos registrada para Santa Teresa é maior que a de todas as demais localidades já inventariadas, em concordância com informações prévias sobre a alta diversidade arbórea e de aves registrada para a região de estudo Palavras-chave: Espírito Santo, inventário, mamíferos, Mata Atlântica Introduction The high biological richness combined with the fast rate of destruction have placed the Tropical forests in the conservation center of attention Estimates show that more than km² of Tropical forests are destroyed each year (Myers, 1997), what represents an enormous lost of biological diversity Although these forests cover only 7% of the earth's surface, they harbor more than half of the biological species (Myers, 1997), most of which still completely unknown The Atlantic forest is one of the most threatened of world's Tropical forests (Mittermeier et al, 1982) Yet, this biome has an enormous biological diversity and a very high degree of endemism, being considered by some authorities as more complex and diverse than several Amazonian sites (Brown & Brown, 1992) The Brazilian mammal fauna has 524 species, making this country the top-ranking in the world Of this total, 250 species occur in the Atlantic forest, 65 species of which are endemics (Fonseca et al, 1996) Rodents and marsupials are especially well represented as 209 species of these two orders occur in Brazil, of which at least 23 marsupials and 79 rodents occur in the Atlantic forest, and 39% and 46%, respectively, are Atlantic forest endemics (Fonseca et al, 1996) In Espírito Santo, a southeastern Brazilian state, the majority of Atlantic forest remnants are fragments isolated in private properties, and the protected areas are, in general, ecologically small Yet, the municipality of Santa Teresa has one of the largest areas covered by native forests, totaling ca 25,000 ha Recently, Thomaz & Monteiro (1997) demonstrated that the Estação Biológica de Santa Lúcia (EBSL), located within the municipality

3 BOL MUS BIOL MELLO LEITÃO (N SÉR ) 11/ of Santa Teresa, has one of the richest community of trees already recorded for the Tropics Although the Atlantic forest has a very diverse fauna with several endemic species (Mittermeier et al, 1982; Fonseca & Kierulff, 1989; Stallings, 1989), its mastofauna is still poorly known, with few localities surveyed exhaustively or subjected to long term studies With the exception of Ruschi (1964, 1965), the first detailed work on small mammals in the montane region of Espírito Santo was conducted by Abravaya (1979), with collections carried out in the Augusto Ruschi Biological Reserve (previously referred to as Nova Lombardia Biological Reserve) Abravaya listed a total of 12 rodent species for that reserve Some information on mammals of EBSL have been reported by Mendes (1991), Passamani & Mendes (1991), Passamani (1996), Chiarello et al (1997) and Chiarello (1998) As remarked by Gargaglioni et al (1998), mammal inventories are extremely important for ecological and behavioral researches, and for the elaboration of management plans for Biological reserves, as species of this group are present in several trophic levels and some species have important roles as seed predators an dispersers This paper presents the partial results of a program for the study of Santa Teresa mammals, including the list of species confirmed for this municipality, as well as a brief discussion on the importance of this region for the preservation of endangered or endemic species Study Area This study was carried out in Estação Biológica de Santa Lúcia and in other Atlantic forest remnants located within the municipality of Santa Teresa, state of Espírito Santo The EBSL (19º 57' S, 40º 32' W) has about 440 ha of area and is administered by the Museu de Biologia Prof Mello Leitão (MBML) Since several neighboring private properties are still heavily forested, however, the reserve's fauna has a total forest area of ca ha The study region is situated between 550 to 950 m of altitude in geomorphological formations of the Cristaline Complex The predominant vegetation in the area is the Montane and Sub-montane Rainy Forest, sensu Rizzini (1979), characterized by non-deciduous trees with leaf buds without protection against drought (Brasil, 1983) The data collected in EBSL between 1957 and 1997 indicates a mean annual precipitation of mm The climate is Cfa of Köeppen's classification, and November is the most rainy month, while June is the only month with mean precipitation below

4 204 PASSAMANI ET AL : MAMMALS OF SANTA TERESA - ES 60 mm (Mendes & Padovan, this issue) Thomaz & Monteiro (1997) estimated a mean annual temperature of 19 9o C, with mean of minimum of 14 3o C and mean of maximum about 26o C A floristic survey carried out in EBSL (Thomaz & Monteiro, 1997), recorded the presence of 443 tree species of 66 families and 178 genera (perimeter at breast height > 20 cm) in a sampling area of 1 02 ha This study also showed that Myrtaceae is the dominant family, with a total of 86 tree species, what represents 19 4% of all sampled species Five new species of trees and possibly a new genus were also found in this area (Thomaz & Monteiro, 1997) Paratypes and holotypes of two new palm species were also collected in EBSL and neighboring areas (Fernandes, 1989; 1996) Methods The mammal inventory was made considering 1) species collected with traps; 2) specimens captured by locals and brought to the MBML; 3) species seen, heard or whose footprints or feces were recorded in the study area during censuses; 4) species that were collected in the Santa Teresa municipality and were deposited in the MBML collection, and 5) published records of species collected in the study region Small mammals were captured from March 1989 to February 1990 The trapping was carried out in various habitats of EBSL using galvanized wire traps of small (29 x 13 x 13 cm) and medium sizes (42 x 2 1x 21 cm), spaced approximately 20 m one from another along transects The traps were placed on the ground, in the lower stratum fixed in tree branches (1-2 m high), and in the medium stratum fixed in tree platforms ( m high) Each morning the traps were baited with banana, pineapple, "Scott Emulsion", peanuts, and sun-dried meat, and were checked the next morning Captured animals were identified, measured, marked with numbered earrings and then released Voucher specimens were taxidermized and deposited in the mammal collection of MBML Medium and large-sized mammals were surveyed with diurnal and nocturnal censuses conducted along several trails of EBSL and in other two reserves located nearby (Estação Biológica de São Lourenço and Reserva Biológica Augusto Ruschi, with ca 500 ha and 3,600 ha, respectively) Occasional censuses have been carried out in EBSL since 1989, and a more regular and intensive census schedule have been carried out in EBSL and in the other two reserves mentioned above by AGC since 1998 During these censuses, the trails were walked slowly ( km/h) during early

5 BOL MUS BIOL MELLO LEITÃO (N SÉR ) 11/ morning (06:00-10:00 h) and early evening (18:00-22:00 h), and a total of 120 km of trails were censused in the three areas (40 km/reserve) The nomenclature used here follows Fonseca et al (1996) Results Mammal species confirmed for EBSL In a total of 21,982 trap night, 21 species of six families were captured during the trapping period, eight of which are marsupials, 12 rodents and one lagomorph (Table 1) Marsupials were the most abundant in the study area, with Gracilinanus microtarsus and Marmosops incanus the species captured most frequently On the basis of direct (visual records) and indirect evidences and through specimens collected in EBSL and deposited in MBML, other 27 mammal species were confirmed for EBSL In total eight orders, 22 families and 48 species were confirmed for this reserve (Table 1) Table 1 Mammal species (excluding bats) confirmed for Estação Biológica de Santa Lúcia with the respective form of detection Species DIDELPHIMORPHIA Didelphidae Marmosops incanus Micoureus demerarae Marmosa murina Gracilinanus microtarsus Metachirus nudicaudatus Didelphis aurita Philander frenata Caluromys philander XENARTHRA (=EDENTATA) Dasypodidae Dasypus novemcinctus Myrmecophagidae Tamandua tetradactyla Detection form MBML collection

6 206 PASSAMANI ET AL : MAMMALS OF SANTA TERESA - ES Species Bradypodidae Bradypus torquatus PRIMATES Callitrichidae Callithrix geoffroyi Callithrix flaviceps Cebidae Alouatta fusca Callicebus personatus Cebus apella CARNIVORA Canidae Cerdocyon thous Procyonidae Nasua nasua Potos flavus Procyon cancrivorus Mustelidae Eira barbara Galictis sp Lontra longicaudis Felidae Leopardus tigrinus Leopardus pardalis Puma concolor PERISSODACTYLA Tapiridae Tapirus terrestris ARTIODACTYLA Cervidae Mazama americana Tayassuidae Pecari tajacu RODENTIA Sciuridae Sciurus aestuans Muridae Akodon cursor Oryzomys intermedius Olygoryzomys nigripes Detection form MBML collection; footprints, footprints, feces Footprints, feces Footprints Footprints, feces Footprints, feces*, footprints, footprints

7 BOL MUS BIOL MELLO LEITÃO (N SÉR ) 11/ Species Oecomys trinitatis Nectomys squamipes Delomys dorsalis Rhipidomys mastacalis Oxymycterus hispidus Caviidae Cavia fulgida Erethizontidae Sphiggurus villosus** Hydrochaeridae Hydrochaeris hydrochaeris Agoutidae Agouti paca Dasyproctidae Dasyprocta leporina Echimyidae Trinomys iheringi Echimys sp Kannabateomys amblyonyx Chaetomys subspinosus LAGOMORPHA Leporidae Sylvilagus brasiliensis Detection form, footprints, feces MBML collection; seen during census * The footprints and feces of tapirs were seen only in July, 1991, but since then no further evidence of the species presence were found in the region ** The specimens seen in Santa Teresa resemble S villosus, but its correct taxonomy needs a more accurate investigation Other mammal species confirmed for Santa Teresa Besides the species recorded in EBSL, 14 additional species were confirmed for the municipality of Santa Teresa, totaling 62 species, including 11 marsupials, six xenarthrans (edentates), six primates, 11 carnivores, one perissodactyl, two artiodactyls, 24 rodents and one lagomorph This total corresponds to approximately 40% of the non-volant mammal species of the Atlantic forest, and 26% of the species (Tables 1 and 2) are Atlantic forest endemics Of the total recorded for the municipality of Santa Teresa, 77% were recorded in EBSL

8 208 PASSAMANI ET AL : MAMMALS OF SANTA TERESA - ES Table 2 Other mammal species (excluding bats) confirmed for the municipality of Santa Teresa with the respective form of detection Species Detection form DIDELPHIMORPHIA Didelphidae Monodelphis scalops Monodelphis americana Chironectis minimus XENARTHRA (=EDENTATA) Dasypodidae Dasypus septencinctus Euphractus sexcinctus Bradypodidae Bradypus variegatus PRIMATES Cebidae Brachyteles arachnoides CARNIVORA Felidae Leopardus wiedii MBML collection MBML collection MBML collection Captured by locals when crossing a road* Seen by Pinto et al (1993) in RBAR** Captured by locals RODENTIA Muridae Akodon sp MBML collection Oryzomys ratticeps Captured by Abravaya (1979) Oryzomys sp MBML collection Blarinomys breviceps MBML collection Delomys sublineatus MBML collection Thaptomys nigrita Captured by Abravaya (1979) * We don t know the exact locality for this specimen, but we have seen B variegatus in Espirito Santo state only in lowlands (below 400 m a s l ) ** RBAR - Reserva Biológica Augusto Ruschi Discussion In this study, we examined the species richness of EBSL and other adjacent areas utilizing capture-recapture techniques, visual records, indirect evidences, as well as the species deposited in the MBML collection The combination of these techniques have been effective to determine accurately the species composition of non-volant mammals, as used in other studies of

9 BOL MUS BIOL MELLO LEITÃO (N SÉR ) 11/ the Tropical region (Eisenberg et al, 1979; Emmons, 1984; Fonseca & Kierulff, 1989; George et al, 1988; Glanz, 1982; Pine, 1973; Rabinowitz & Nottingham, 1989; Stallings, 1989) This list is still preliminary, however, as further studies utilizing additional kind of traps, sampling in other areas, as well as more intensive censuses in all habitat types, would certainly reveal additional species Also, if Chiroptera were included, the species richness of the study region would increase substantially, since bats, together with rodents, dominate the mammal diversity in the Tropics (Fleming, 1975; Eisenberg, 1978; Voss & Emmons, 1996) The number of mammal species recorded for EBSL demonstrates a high species richness, and, importantly, the majority of these species are listed for the first time in the region Deserves mention the presence of nine species included in the Brazilian list of endangered species of mammals (Fonseca et al, 1994); some of which have been the subject of detailed ecological and behavioral studies, such as Callithrix flaviceps (Mendes, 1993), Chaethomys subspinosus (Chiarello et al, 1997), and Bradypus torquatus (Chiarello, 1998a,b) In the Santa Teresa region, marsupials and rodents had the highest richness of species, representing 50% and 30% of the Atlantic forest species, respectively (Fonseca et al, 1996) With the exception of the Manu Biosphere Reserve, Peru (Pacheco et al, 1993), the richness of marsupial and rodent species recorded for Santa Teresa is higher than that reported for other Neotropical sites Considering also the other orders, only Manu Biosphere Reserve and Belém have higher number of mammal species than Santa Teresa (Table 3) As remarked by Voss & Emmons (1996), the comparison of species lists among study sites is difficult since both methods and sampling effort vary among studies This is specially true for the other Atlantic forest sites, whose inventories are far from complete It is likely that more detailed studies carried out in other Atlantic forest sites would reveal equally or perhaps even higher, species richness than that reported from EBSL Nevertheless, the data currently available do suggest that Santa Teresa is special in terms of biodiversity, since the richness of mammals found in this region is mirrored by its equally rich bird (Simon, this issue), and tree communities (Thomaz & Monteiro, 1997) Why this is so remains an unanswered question, but is probably related to a combination of favorable biotic and abiotic factors, including the region's topographic and edaphic heterogeneity, and its mild weather, which is characterized by the lack of severe dry seasons, frosts, or extremely hot temperatures

10 210 PASSAMANI ET AL : MAMMALS OF SANTA TERESA - ES Table 3 - Number of mammal species (excluding bats, cetaceans and sirenians) recorded for some Tropical forest sites Barro Sierra de La Selva Cockscomb Manu Tapajós Manaus Belém Rio Doce Fazenda Itatiaia Santa Colorado Chama Costa Rica1 Basin Biosphere Amazonas Amazonas Pará Minas Ipanema Rio de Teresa Island, Guatemala 2 Belize 3 Reserve Brazil 5 Brazil 1 Brazil 6 Gerais São Paulo Janeiro Brazil Panama 1 Brazil 7 Brazil 8 Brazil 9 (this study) PredominantTropical Montane Tropical WetSub- Amazon Amazon Amazon Amazon Atlantic Atlantic Atlantic Atlantic Vegetation Forest Tropical Forest tropical ForestForestForestForestForestForestForestForest ForestForest Altitude (m) 90? ? Didelphimorpha Xenarthra Primates Carnivora Perissodactyla Artiodactyla Rodentia Lagomorpha Total Compiled by Voss & Emmons, 1996; 2 Hendrichs, 1978; 3 Rabinowitz & Nottinghan, 1989; 4 Pacheco et al, 1993; 5 George et al, 1988; 6 Pine, 1973; 7 Stallings et al, 1991; 8 Pelzeln, 1883; 9 Ávila-Pires & Gouvêa, 1977

11 BOL MUS BIOL MELLO LEITÃO (N SÉR ) 11/ Although the Atlantic forest in Espírito Santo and in Brazil is reduced to less then 10% of its original extend (Câmara, 1991), the Santa Teresa municipality has a privileged conservation status since more then 25%, and perhaps almost 40%, of its surface area is still covered with native forests (Tabacow, 1992; Mendes e Padovan, this issue) The majority of forest remnants of this region are not completely isolated in private properties since the remnants are relatively close to each other, and the area officially protected includes ca 5,000 ha The connectivity of these forest remnants is increased by an abundance of Eucalyptus plantations, which allow the movements of species with high requirements of space, such as pumas (Puma concolor), tapirs (Tapirus terrestris), and collared-peccaries (Tayassu pecari) It is important to mention, however, that tapirs and pumas were only occasionally recorded in EBSL, suggesting that these species might be using the area of this reserve for movements to and from other forest remnants in the region In Santa Teresa, puma footprints are relatively abundant only in Reserva Biológica Augusto Ruschi (ca 3,600 ha), the only reserve in this region that still have a resident population of collared-peccaries, one of the cat's main prey Probably, the presence of peccaries, together with capybaras (Hydrochaerys hydrochaerys) and pacas (Agouti paca), which are abundant in this reserve, might explain why pumas still survive in the reserve's area Regarding tapirs, however, no convincing evidence of the species presence in the whole region of Santa Teresa has been recorded in the last nine years, suggesting that tapirs might be locally extinct or have a drastically reduced population size It is likely that several Atlantic forest species are disappearing before we could understand their role or importance in the forest ecosystem, and some might even be extinguished without been known by scientists Therefore, it is of fundamental importance that more research be conducted in order to provide the necessary information and to allow that management and conservation actions be implemented to help preserve the species and the environment as a whole Acknowledgements We wish to thank the logistical help provided by all the staff of Museu de Biologia Prof Mello Leitão and to the CNPq for fellowships of M Passamani (# /97-5) and A G Chiarello (# /98-0) Wilson Hoffmann, Elias Bausen, Jenilson Dalmaschio and Rogério R Santos

12 212 PASSAMANI ET AL : MAMMALS OF SANTA TERESA - ES helped with data collection of small mammals, and Bernardo Brito and Marlon Zortéa kindly confirmed the presence of some species Marcelo Weksler and João Alves de Oliveira identified some rodent species References ABRAVAYA, J P 1979 Population Ecology of some Brazilian Rodents MSc Thesis California State University, Northrigde ÁVILA-PIRES, F D & GOUVÊA, E 1977 Mamíferos do Parque Nacional de Itatiaia Bol Mus Nacional, (N Ser ), 291: 1-29 BRASIL 1983 Departamento nacional de produção mineral Projeto RADAM V 32 Folhas SF23/24 Rio de Janeiro/Vitória, Rio de Janeiro CÂMARA, I G 1991 Plano de Ação para a Mata Atlântica Ed Interação Ltda, São Paulo CHIARELLO, A G 1998a Activity budgets and ranging patterns of the Atlantic forest maned sloth Bradypus torquatus (Xenarthra: Bradypodidae) J Zool, Lond, 246: 1-10 CHIARELLO, A G 1998b Diet of the Atlantic forest maned sloth, Bradypus torquatus (Xenarthra: Bradypodidae) J Zool, Lond, 246:11-19 CHIARELLO, A G, PASSAMANI, M & ZORTÉA, M 1997 Field observation on the thin-spined porcupine, Chaetomys subspinosus (Rodentia; Echimyidae) Mammalia, 61: EISENBERG, J F 1978 The density and biomass of tropical mammals In: M Soulé & B Wilcox (eds ) Conservation Biology Sinauer Assoc Inc, Sunderland, p EISENBERG, J F, O'CONNELL, M & AUGUST, P V 1979 Density, productivity, and distribution of small mammals in two Venezuelan habitats In: J F Eisenberg (ed ) Vertebrate Ecology in the Northern Neotropics Smithsonian Institution Press, Washington, p EMMONS, L H 1984 Geographic variation in densities and diversities of non-flying mammals in Amazonia Biotropica, 16: FERNANDES, H Q B 1989 Uma nova espécie de Euterpe (Palmae- Arecoideae-Arecacea) do Brasil Acta Bot Brasil, 3: FERNANDES, H Q B 1996 Bactris timbuiensis (Palmae), uma espécie nova da Mata Atlântica no Espírito Santo, Brasil Bol Mus Biol Mello Leitão, (N Ser ), 5:3-14

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